Facultative Cleaner Species in Marine Temperate Waters: the Ecological Role of Juvenile Diplodus Sargus (Sparidae)
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Facultative cleaner species in marine temperate waters: the ecological role of juvenile Diplodus sargus (Sparidae) José Nuno de Oliveira Neto Nº 24378 Thesis supervisor: Prof. Doctor Frederico Almada Thesis seminar supervisor: Prof. Doctor Emanuel Gonçalves In partial fulfillment of the requirements for the degree of MASTER IN MARINE BIOLOGY AND CONSERVATION 2017 Thesis under the supervision of Prof. Doctor Frederico Almada, for the attainment of the degree of masters in Marine Biology and Conservation 1 TABLE OF CONTENTS List of tables ............................................................................................................................................ 3 List of figures ........................................................................................................................................... 4 List of appendices .................................................................................................................................. 5 1. Introduction ......................................................................................................................................... 6 2. Methodology ....................................................................................................................................... 8 3. Results ................................................................................................................................................... 10 I. Cleaning events, Nips and Duration ....................................................................................... 10 II. Client fish ....................................................................................................................................... 12 III. Client reaction ............................................................................................................................. 13 IV. Cleaner preference...................................................................................................................... 15 V. Focal observations ....................................................................................................................... 16 4. Discussion............................................................................................................................................ 17 5. References ............................................................................................................................................ 26 6. Appendices .......................................................................................................................................... 31 2 LIST OF TABLES Table 1. Distribution of cleaning interactions by D. sargus according to host species ........................................................ 12 Table 2..Visual census ..................................................................................................................................................................... 15 Table 3. Diplodus sargus cleaning frequencies between clients .............................................................................................. 21 Table 4. Centrolabrus exoletus cleaning frequencies between clients ................................................................................... 22 Table 5. Symphodus melanocercus cleaning frequencies between clients ............................................................................ 23 Table 6. Cleaning rates of Facultative and Obligatory cleaners in temperate waters .......................................................... 24 3 LIST OF FIGURES Figure 1. Schematic representation of the cleaner-client interactions between D.sargus and its clients ......................... 10 Figure 2. Number and outcome of all visual inspections (Failed interactions and cleaning events) ................................ 11 Figure 3. Daily pattern of cleaning events, nips and duration of cleaning events ............................................................... 11 Figure 4. Correlation between number of nips and duration of cleaning events ................................................................ 12 Figure 5. Reaction to nips according to cleaner size ................................................................................................................. 14 Figure 6. Reaction to nips according to client size .................................................................................................................... 14 Figure 7. Targeted section of client body according to cleaner size ...................................................................................... 16 4 LIST OF APPENDICES Appendix I. State-of-the-art .......................................................................................................................................................... 31 Appendix II Sampling locations ................................................................................................................................................... 45 Appendix III Visual classification of the Diplodus genera ........................................................................................................ 47 5 1. Introduction Cleaning symbiosis is an association, during which, an organism defined as “cleaner” removes parasites, dead tissue or unwanted food particles from the epidermis of a co-operating “client” (Galeote & Otero, 1998). This behaviour is found in a variety of terrestrial vertebrates, but is especially common within marine ecosystems. Although they were first noted as being episodic, events of cleaning symbiosis in marine environment are now considered to be a regular occurrence of ecological relevance(Limbaugh, 1961; Grutter, 1999), with over a hundred species of fish already reported as cleaners (Van Tassell et al., 1994; Arnal et al., 2006). According to their behavior, cleaner fish are classified as facultative or obligatory cleaners. While species from the first group exhibit this behaviour during a specific phase of their life-cycle and rely on other food sources for their diet, fishes on the second group depend mostly on their success obtaining food from these interactions during their entire lifespan (Arnal & Côté, 2000). Due to this and other factors intrinsic to each ecosystem, the frequency and periodicity of cleaning interactions may vary greatly amongst species (Floeter et al., 2007). Besides the relative importance of cleaning interactions as food source and general difference in cleaning rates between obligatory cleaners and facultative ones, obligatory cleaners seem to share some morphological characteristics. Physical traits such as small body size and contrasting striped patterns are common among obligatory cleaners, which may help clients choosing their cleaners through visual cues (Stummer et al., 2004). Regardless the number of species currently described as cleaners, the ecological relevance of cleaning interactions has been frequently debated (Cheney & Côté, 2005). Difficulties assessing client gain during these interactions, while cleaners benefits remain obvious raised doubts whether these interactions should be consider parasitism, commensalism or mutualism (Cheney & Côté, 2005). Episodes of cheating during cleaning activity, with “cleaners” biting healthy tissue from their clients, resulting in mucus loss, and tissue injuries, have been repeatedly described (Bshary & Schäffer, 2002; Grutter & Bshary, 2003). However clients seem to actively choose the cleaners they interact with in order to avoid these occurrences (Bshary & Schäffer, 2002; Bshary & Grutter, 2005; Pinto et al., 2011). Furthermore, while cleaners tend to be sedentary, defending small territories within which they display this behaviour, many clients have a roaming lifestyle, and visits to these cleaning stations may represent a risk of being preyed upon (Cheney & Côté, 2001; Oates et al., 2012). In any case, cleaning interactions have an impact on the ecological relationships between clients and cleaners. Several studies indicate that cleaners choose their clients based upon their 6 parasite loads, and that the size and number of parasites of the clients are directly affected by these interactions (Grutter, 1995; Grutter, 1999; Arnal et al., 2000). Field experiments have shown that completely removing cleaners from specific reefs, impacts the community within the ecosystem, with several fish opting to roam into other areas (Limbaugh, 1961; Bshary, 2003). This highlights the ecological importance of cleaners as key organisms within their respective communities (but see Grutter, 1996a). However, cleaning behaviour has been frequently studied in tropical fishes and few studies where made concerning species in temperate regions (Limbaugh, 1961; Van Tassell et al., 1994; Galeote & Otero, 1998). Most cleaner species belong to the families Labridae and Gobiidae with a worldwide distribution (Arnal et al., 2006; Baliga & Law, 2016) and there is no trend supporting the assumption that this behaviour is more frequent in tropical waters (Hobson, 1968). Main cleaner species according to their geographical distribution include, among the Labridae, Labroides dimidiatus in the Indic and Pacific Ocean (Grutter, 1997), Symphodus melops (Potts, 1973) and Centrolabrus exoletus in the north-eastern Atlantic (Henriques & Almada, 1997), and Centrolabrus melanocercus in the Mediterranean Sea (Weitzmann & Mercader, 2012; Zander & Sötje, 2002). However, the increase of observations in temperate